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Carbon and Nitrogen Acquisition in Shallow and Deep Holobionts of the Scleractinian Coral S Carbon and Nitrogen Acquisition in Shallow and Deep Holobionts of the Scleractinian Coral S. pistillata Leïla Ezzat, Maoz Fine, Jean-François Maguer, Renaud Grover, Christine Ferrier-Pagès To cite this version: Leïla Ezzat, Maoz Fine, Jean-François Maguer, Renaud Grover, Christine Ferrier-Pagès. Carbon and Nitrogen Acquisition in Shallow and Deep Holobionts of the Scleractinian Coral S. pistillata. Frontiers in Marine Science, Frontiers Media, 2017, 4, pp.UNSP 102. 10.3389/fmars.2017.00102. hal-02572876 HAL Id: hal-02572876 https://hal.archives-ouvertes.fr/hal-02572876 Submitted on 13 May 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. ORIGINAL RESEARCH published: 13 April 2017 doi: 10.3389/fmars.2017.00102 Carbon and Nitrogen Acquisition in Shallow and Deep Holobionts of the Scleractinian Coral S. pistillata Leïla Ezzat 1*, Maoz Fine 2, 3, Jean-François Maguer 4, Renaud Grover 1 and Christine Ferrier-Pagès 1 1 Marine Department, Scientific Centre of Monaco, Monaco, Monaco, 2 The Mina and Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat-Gan, Israel, 3 The Interuniversity Institute for Marine Sciences, Eilat, Israel, 4 Laboratoire de l’Environnement Marin, UMR 6539, UBO/Centre Nationnal de la Recherche Scientifique/IRD/IFREMER, Institut Universitaire Européen de la Mer, Plouzané, France Reef building corals can host different symbiont genotypes (clades), and form distinct holobionts in response to environmental changes. Studies on the functional significance of genetically different symbionts have focused on the thermal tolerance rather than on the nutritional significance. Here, we characterized the nitrogen and carbon assimilation rates, the allocation patterns of these nutrients within the symbiosis, and the trophic condition of two distinct holobionts of Stylophora pistillata: one associated with Edited by: Symbiodinium clade A in shallow reefs and the other one associated with clade C in Noga Stambler, mesophotic reefs. The main findings are that: (1) clade C-symbionts have a competitive Bar-Ilan University, Israel advantage for the acquisition of carbon at low irradiance compared to clade A-symbionts; Reviewed by: Susana Enríquez, (2) light is however the primary factor that determines the positive relationship between National Autonomous University of the amount of carbon fixed in photosynthesis by the symbionts and the amount of Mexico, Mexico carbon translocated to the host; and (3) by contrast, the dominant Symbiodinium type Michael P. Lesser, University of New Hampshire, USA preferentially determines a negative relationship between rates of coral feeding and David Michael Baker, nitrogen assimilation, although light still plays a relevant role in this relationship. Clade University of Hong Kong, Hong Kong C-holobionts had indeed higher heterotrophic capacities, but lower inorganic nitrogen *Correspondence: Leïla Ezzat assimilation rates than clade A-holobionts, at all light levels. Broadly, our results show leila@centrescientifique.mc that the assimilation and translocation rates of inorganic carbon and nitrogen are clade and light-dependent. In addition, the capacity of S. pistillata to form mesophotic reefs in Specialty section: the Red Sea relies on its ability to select Symbiodinium clade C, as this symbiont type is This article was submitted to Coral Reef Research, more efficient to fix carbon at low light. a section of the journal Frontiers in Marine Science Keywords: light acclimation, carbon isotopes, nitrogen isotopes, clades, nitrate, ammonium, scleractinian coral, mesophotic coral Received: 14 December 2016 Accepted: 27 March 2017 Published: 13 April 2017 INTRODUCTION Citation: Ezzat L, Fine M, Maguer J-F, Grover R Coral reefs support one of the most diverse and productive biological communities on Earth. Their and Ferrier-Pagès C (2017) Carbon success owe from the symbiotic relationship that corals build with photosynthetic dinoflagellate and Nitrogen Acquisition in Shallow and Deep Holobionts of the algae, commonly named zooxanthellae, that can sustain up to 95% of the daily energetic demand of Scleractinian Coral S. pistillata. the symbiotic association (Muscatine et al., 1984; Muscatine, 1990), also called holobiont (Rohwer Front. Mar. Sci. 4:102. et al., 2002). While symbionts need light for photosynthesis and constrain their host to mainly doi: 10.3389/fmars.2017.00102 develop in the first 30m depth, corals can however form large structures called mesophotic reefs Frontiers in Marine Science | www.frontiersin.org 1 April 2017 | Volume 4 | Article 102 Ezzat et al. Nutrient Acquisition in Mesophotic Corals in much deeper waters. Mesophotic reefs therefore refer to deep heterotrophic capacities of the host (Leal et al., 2015). Overall, but light-limited coral ecosystems (Hinderstein et al., 2010), these studies suggest that symbiont identity directly relates to ranging between 30 and 80m in the Gulf of Mexico (Kahng, the trophic plasticity of the holobiont. Because acquisition of 2010), to more than 100 m in some locations with exceptionally both auto-and heterotrophic nutrients is critical for coral growth clear waters, such as the Red Sea (Lesser et al., 2009; Winters and reproduction (Muscatine and Porter, 1977; Muscatine et al., et al., 2009). Although, photosynthesis is limited by the low light 1989; Ferrier-Pages et al., 2000; Houlbreque and Ferrier-Pagès, levels, these reefs host a wide diversity of taxa due to numerous 2009), a better understanding of the nutritional capacities of upwelling events and internal waves, that deliver significant different holobionts will help predict their resilience to stress. amounts of inorganic nutrients and particulate organic matter Until now, no direct simultaneous comparison exists between (Leichter and Genovese, 2006; Lesser et al., 2009). auto-and heterotrophic performance of shallow and deep corals In response to decreased light intensity, corals can either associated with different Symbiodinium genotypes, although deep present host (Brazeau et al., 2013) and/or symbiont genetic reefs host a huge biodiversity (Hovland, 2008). diversity (Lesser et al., 2010) as well as adaptations to grow under Here we compare the trophic and photosynthetic capacities low irradiance conditions. For example, in order to increase of two distinct holobionts of the scleractinian coral S. pistillata and optimize the light capture and rates of autotrophic carbon living in shallow and mesophotic reefs of Eilat (Red Sea). production at depth >30 m, corals undergo morphological S. pistillata, harbors clade A1 in shallow waters (<40 m) and changes (Mass et al., 2007; Einbinder et al., 2009; Nir et al., clade C in deeper environments (>40 m), forming two different 2011) as well as modifications in the photo-physiological traits of holobionts of the same species (Byler et al., 2013). We measured, their symbionts (Wyman et al., 1987; Lesser et al., 2000, 2009). under the light conditions of surface and deep waters, the They also compensate their low photosynthate production by heterotrophic capacities of each holobiont, as well as their increasing the acquisition of heterotrophic nutrients (Muscatine rates of photosynthesis and acquisition of inorganic carbon 13 13 15 et al., 1989; Mass et al., 2007; Alamaru et al., 2009; Einbinder and nitrogen using stable isotopes [NaH CO3 ( C), NH4Cl 15 et al., 2009; Lesser et al., 2010; Crandall et al., 2016). Corals (NH4), and NaNO3 (NO3)]. Inorganic carbon and nitrogen can finally harbor different Symbiodinium clades depending on acquisition by the symbionts, together with host prey capture, the depth at which they thrive (Finney et al., 2010; Lesser provide direct measures to score nutritional plasticity of these et al., 2010). In the Caribbean, although some colonies can symbioses. Getting new insights into the trophic behavior and the present a mix of symbiont clades with a zonation pattern metabolic processes associated with mesophotic corals is essential (Kemp et al., 2015), Symbiodinium A and B are predominant to understand the ecology and biology of these unique habitats in tissue exposed to high irradiance (surface waters) while as well as the vertical connectivity existing between shallow and Symbiodinium C is dominant in shaded tissue of deep corals deep environments, which may be of great importance for the (Rowan and Knowlton, 1995; Rowan et al., 1997). In the northern future health and resilience of their associated ecosystems. Red Sea, Stylophora pistillata shifts from hosting clade A in shallow waters to clade C below 40 m depth (Mass et al., MATERIALS AND METHODS 2007; Winters et al., 2009). Although, numerous studies have now acknowledged the diversity and flexibility of Symbiodinium Biological Material and Experimental Setup under different light environments, the functional significance of Experiments were performed in November 2014 at the IUI, in these associations remains unexplored. It has been suggested that the Gulf of Eilat (Israel). While light conditions decreased from physiological diversification in Symbiodinium species
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